Tuesday, July 26, 2016

How
fish have changed my understanding of evolution, and how they brought me to the
field of eco-evolutionary processes, particularly to study how species-specific
factors can shape fishing-induced selection

When I started studying evolution, about 20
years ago, things were relatively simple; individuals differed in some
phenotypic trait and environmental conditions would fuel natural selection and
select for the most successful individuals in such an environment. It had been
well described about a hundred years ago, by a famous English bearded
naturalist named Charles Darwin, and it was sufficiently simple that it could
be applied to everything I knew in biology.

I later discovered that it was a little more
complex, as it is in fact genes that respond to selection, and not directly
individuals, thanks to another English evolutionist, a hairy one, Richard
Dawkins [1]. Nothing
really perturbing when you preach to the choir, just a slight scale adjustment.

But after that, I started to work on fish
and everything changed…

First, I discovered phenotypic plasticity;
which means that your environment could completely modify your appearance and
that one genetic combination could result on a vast array of traits. I
particularly appreciate how the owner of this blog illustrates that phenomenon
by regularly modifying his facial hair template (sorry Andrew, but you knew
somebody would eventually collect all these pictures…).

Beside this Homo
sapiens case, one of the most fascinating examples of phenotypic plasticity
is how trout (brown trout or rainbow trout) can stay in their native river and
become resident, or can move downstream (in lakes, sea, or ocean) and become
enormous in a few years. Even more dramatic, also debatable if this is truly
plasticity, some clownfish will change their sex when the dominant female dies.
For the young evolutionary biologist that I was, it implied an immense adjustment
to my system of thoughts, and it had big consequences on how selection and
environmental processes interacted. Sometimes, it’s not the phenotype that is
selected for, but how well the phenotype can be adapted to be more fit. Studies on bichir fish (Polypterus sp.) have even suggested that plasticity could be a
source of evolution [2,3], i.e., that when individuals experience a
dramatic environmental change (such as migrating from sea to land), their body could
change without mutation involved (in this case they learned to walk), and
natural selection will only then favor mutations to fix this transition.

Another consequences of plasticity, sympatric
speciation, brought me to the next puzzling conundrum implying evolving fish.
Sympatric speciation means that from one founding, relatively homogeneous,
population, several new species can flourish in the same environment. Meaning
that in a particular environment, several paths could be taken by evolution to
reach a stable state, and from one initial population, different genes
combinations could be best adapted to such particular environment. This is very
puzzling, as individuals sharing the same space shouldn’t become sexually
separated, but still there is plenty of work, and particularly on cichlids,
that demonstrate its reality [4]. These cichlids evolved into many different species,
and this process could even be replicated in different lakes!

Much closer to me, both in terms of
location and species of interest, is the adaptive radiation of alpine whitefish[5].
Almost every lake in Switzerland has several species of whitefish, usually one
fast growing species specializing on larger preys (benthic fauna), and one slow
growing species specializing on smaller preys (zooplankton). These “species”
are still very close genetically, and can interbreed under some conditions, so
they should be considered an intermediate step between morphs and species. Interestingly,
the genetic distance between these populations is smaller between two morphs in
the same lake than between the same morphs in two different lakes. Most
stunningly, this evolution towards different morphs happened so recently, that
it shouldn’t be even conceivable. Lakes in Switzerland were frozen during the
last glaciation, some 10’000 years ago, so this specialization was extremely
rapid (evolutionarily speaking). This question of rapid evolution was one of
the biggest revelations of my early career, evolutionary processes did not have
to wait millions of years to be meaningful, but instead could be as rapid as
ecological processes! I guess that you have a good idea of where I am going…
Are there any interactions between both? And if yes how does it work? I spent
the last ten years trying to understand these questions by studying how
environmental factors could shape the response to fishing-induced selection.

During my PhD work in Switzerland, I measured
change in growth through time in several Alpine whitefish populations, and
contrasted it with estimations of selection differentials on growth. I found
out that both ecological (phosphorus change) and evolutionary processes
(fishing selection) where involved in the growth decreases observed. However, and
very interestingly, the contribution of both processes was very variable. Fishing-induced
selection could explain between 20 and 70 percent of the change observed in
growth and this contribution was mediated by ecological processes, such as the
trophic state of the lake, and species-specific processes, the type of life-history
(slow or fast growers).

This interaction between harvesting, species-specific
parameters, and fishing-induced evolution has been modeled by Erin Dunlop, Anna Eikeset and Nils Stenseth[6], and
we found it so interesting that we spotlighted their research in the latest TREE edition[7].
Their model explores how the
interaction between species life-history speed and selection for earlier
maturation can impact the population growth rate and therefore the stock
productivity. They contrasted the outcomes of fishing on three harvested
fish species, characterized by different life histories: Atlantic cod (Gadus morhua) with a “slow” life
history, lake whitefish (Coregonus
clupeaformis) with intermediate” life history, and yellow perch (Perca flavescens) with “fast” life-history.
They used individually-based simulations that modeled the fisheries-induced
evolutionary change of the probabilistic maturation reaction norm (PMRN), which
describes the maturation probability given a certain age and size. In
particular, they measured how the evolvability of the maturation parameters,
the fishing intensity, and the strength of density dependence interacted to
influence population growth rate.

Their study describe that, under the
influence of fishing, the population growth rate follows what we called a
transient dynamic, i.e., fishing had a reducing effect on population growth
rate when fishing starts (with the removal of the largest individuals), and that
reduction is followed by a recovery as density-dependent processes lead to
increase growth (overcompensation). When fishing stops, after the introduction of
a moratorium for example, they observed a reversed transient dynamic, i.e., an
increase in growth rate due to the suppressed harvesting of the largest fish,
followed by a compensatory density-dependent response when the population
reaches carrying capacity. This transient dynamic after fishing cessation was
highly influenced by fishing-induced evolution, but in a species-specific way. Species
with slow life-histories can “adapt” to fishing by maturing at an earlier age,
which reduces the risk of collapse during fishing but also induces a genetic
legacy that impairs recovery during moratoria. On the other hand, for species
with fast life histories, they observed a reduced impact of FIE, as fast
growing species were already reproducing as early as possible. The consequences
for these species was a faster recovery during moratoria, due to the reduced
genetic legacy, but at the cost of an increased risk of collapse at high
harvest rates as such species could not adapt to fishing.

Such impact of species-specific factors might
explain the discrepancy observed in studies investigating the response to
size-selective fishing; or why some species with slow life histories that have experienced
high harvest rates have shown slow recoveries even after several years of
fishing moratoria. Understanding how and when evolutionary change matters are
key management questions but are problematic as each population can respond
differently. I believe that disentangling how environmental and
species-specific factors influence the response to size-selective fishing is
the next step necessary to develop robust management policies.